Int. J. Agron. Agri. R.
International Journal of Agronomy and Agricultural Research (IJAAR) ISSN: 2223-7054 (Print) 2225-3610 (Online) http://www.innspub.net Vol. 12, No. 1, p. 62-68, 2018 OPEN ACCESS
RESEARCH PAPER
Diversity of plant parasitic nematodes associated with common beans (Phaseolus vulgaris) in the Central Highlands of Kenya J. W. Waceke*
Department of Agricultural Science and Technology, Kenyatta University, Nairobi, Kenya Article published on January 30, 2018 Key words: Meloidogyne, Pratylenchus, Gall index, Disease severity, PPN densities
Abstract Common beans (Phaseolus vulgaris L.) are the most important legume staple food in Kenya coming second to maize. In Central Highlands of Kenya, the 0.4-0.5ton ha-1 output is below the genetic yield potential of 1.5-2ton ha-1 partly due pests and diseases. Plant parasitic nematodes (PPN) have been reported to cause yield losses of up to 60% on beans. Though bean production is important in the Central highlands of Kenya, information on PPN associated with the beans in the region is lacking. This study was therefore undertaken to establish the diversity of PPN associated with common beans and to assess the root knot nematode damage on beans in the region. The study covered 50 farms (32 in Kirinyaga and 18 in Embu Counties) distributed in eight localities namely Kibirigwi (L1), Makutano (L2), Kagio (L3), Mwea (L4) and Kutus (L5) in Kirinyaga County and Nembure (L6), Manyatta (L7) and Runyenjes (L8) in Embu County and covering three Agro Ecological Zones (AEZs); UM2 (L1, L2, L3 & L4), UM3 (L5, L7 & L8) and UM4 (L6) AEZs. Manyatta (L7) and Nembure (L6), had the highest and second highest gall indices, respectively, while Kibirigwi (L1), Makutano (L2) and Mwea (L4) had some of the lowest gall indices. The most common PPN in bean roots were Meloidogyne spp. Pratylenchus spp. and Scutellonema spp. with a frequency of 94.38%, 78.25% and 59.13%, respectively. This further confirm the importance of these nematodes in bean production systems. Upper Midland 3 (UM3) AEZs and UM4 had higher nematode population densities and diversity than UM2. Disease severity and nematode composition and distribution were notably low in the irrigated areas Kibirigwi, Kagio and Mwea compared to rain-fed areas such as Makutano, Nembure and Manyatta. * Corresponding
Waceke
Author: Waceke J.W  wanjohi.waceke@ku.ac.ke
Page 62
Int. J. Agron. Agri. R. Introduction
associated with common beans and assess the root
Common beans (Phaseolus vulgaris L.) are the most
knot nematode damage on beans in the Central
important legume staple food in Kenya providing up
highlands of Kenya.
to 65 percent of the country’s national dietary protein intake and 32 percent of caloric intake (Wortmann &
Materials and methods
Allen 1994). Due to their capacity to fix nitrogen they
Study Area
are frequently used in maize cropping systems as an
The study was conducted in Kirinyaga and Embu
intercrop and reduces dependence on inorganic N
Counties in the Central Highlands of Kenya. These
fertilizers (Rheenen et al., 1981). In the central
counties lie on the foot of Mt. Kenya at 1280 - 2500m
highlands of Kenya, though bean production is an
above sea level. The climate is cool and humid\sub-
importance economic activity where it covers over
humid with an annual mean temperature of 20-21ď‚°C.
40000 hectares and, the yield of 0.5ton
ha-1
is far
This region has a bimodal rainfall pattern with peaks
below the genetic yield potential of 2ton ha-1 (Katungi
in May and November and a hot dry spell between
et al., 2010). These low yields are attributed to low
January and April. Average annual rainfall for this
soil fertility, diseases and insect pests as revealed by a
area is 1250mm in the higher altitudes. In lower
study conducted in 2015 in parts of the region
altitudes the rainfall decreases and the rainy seasons
(Mwaniki 2015). The bean diseases were ranked as
become shorter. Soils are deeply weathered volcanic
the most important (87.5%), followed by low soil
types mainly andosols in Upper Midland 2 (UM2) and
fertility (52.5%), insect pests (50%), lack of quality
nitosols in Upper Midland 3 (UM3) and Upper
seed (17.5%), low market prices (12.5%) and erratic
midland 4 (UM4) agro-ecological zones (AEZ)
weather patterns (10%) (Mwaniki, 2015). Although a
(Jaetzold and Schmidt, 1983).
study on the distribution and population densities of PPN associated with beans in Western Kenya revealed
The study covered 50 farms (32 in Kirinyaga and 18
that PPN are a big threat to bean production (Karanja
in Embu Counties) distributed in eight localities
et al., 2003), studies conducted in the central
namely Kibirigwi (L1), Makutano (L2), Kagio (L3),
highlands of Kenya often overlook the impact on PPN
Mwea (L4) and Kutus (L5) in Kirinyaga County and
on beans production. In other regions, plant parasitic
Nembure (L6), Manyatta (L7) and Runyenjes (L8) in
nematodes have been reported to cause yield losses of
Embu County. The farms were concentrated in the
up to 60% with root knot nematodes being rated as
UM2 (L1, L2, L3 & L4), UM3 (L5, L7 & L8) and UM4
the most important (Talwana et al., 2016; Kavuluko et
(L6) AEZs where cultivation of bean is most common.
al., 2010; Kimenju et al., 1999). In addition to direct
Though bean production is mainly rain fed, farms in
pathogenic effects on plants, the nematodes act
three localities; L1, L3 and L4 irrigate their crops
synergistically with other plant pathogens and pests
since most of them are under Kibirigwi and Mwea
to form disease complexes that further impact
Irrigation Schemes. In most farms, beans were inter-
negatively on the crops. The nematodes also suppress
cropped with maize.
nodulation and therefore affect nitrogen fixation (Kimenju
et
al.,
1999).
Information
on
PPN
Sampling
associated with common beans in Central Highland of
Samples were collected in the middle of the short rain
Kenya is lacking. Further, due to the growing
season October - November 2015. Ten bean and soil
importance of bean production in the region, it is
samples per farm were taken at mid-season when the
imperative that a study be undertaken assess the
bean plants were in the early poding stage. The farms
diversity of PPN associated with beans in an effort to
were selected with the assistance of the County
applying sound management and control strategies.
Executive Committee (CEC) offices in charge of agriculture in the two counties. The plants were
This study was therefore undertaken to establish the
gently dug out with a hand hoe taking care not to
occurrence and diversity of plant parasitic nematodes
damage the roots. Soil adhering on the roots was
Waceke
Page 63
Int. J. Agron. Agri. R. gently shaken off into a plastic bag, then the root
(Hooper et al., 2005) Nematode suspension from the
system was separated from the shoot system and
tray was sieved through a 38m sieve every day for 3
cleaned before assessing the gall index and extracting
days. The nematodes were backwashed into a beaker
the nematodes. The soil samples for each farm were
and concentrated into a 20ml suspension and placed
1000cm3
in vials. Nematodes were enumerated under a
bulked, mixed thoroughly before taking a for nematode assays
dissecting microscope and density and frequency of occurrence determined.
Assessment of disease severity Nematode damage on the bean plant was assessed by visually rating the roots for galls using the Bridge and Page (1980) gall rating of 0-10 where 0= No knots on roots; 1= Few small knots that are difficult to find; 2=Small knots only but are clearly visible and main roots clean; 3= Some larger knots are visible and main roots clean; 4=Larger knots pre-dominate but main roots clean; 5=50% of roots infested and knotting on parts of main root and reduced root; 6=Knotting on main root; 7=Majority of main roots knotted; 8=All main roots knotted but few clean roots visible; 9=All roots severely knotted and plants usually dying and 10=All roots severely knotted and
Results and discussion Nematode galling index The most distinct symptom of nematode damage on the bean plants was root galling by Meloidogyne spp. Root Knot nematode damage levels varied in the 8 localities with Manyatta (L7) and Nembure (L6), having the highest and second highest gall indices, respectively. Kibirigwi (L1), Makutano (L2) and Mwea (L4) had some of the lowest gall indices of 1.17, 1.25 and 1.3, respectively, that differed significantly (p<0.05) from those in locality 7. Farms in localities 3, 5 and 8 had gall indices of 1.5 (Fig. 1).
no root system and plant usually dead. Extraction of Nematode from bean roots The cleaned root systems from each farm were cut into 1cm long pieces, were well mixed before taking two 5g sub samples. One sub -sample was oven dried for 72 hours at 60C while the second one was used for nematodes extraction using Maceration-Filtration method (Hooper et al., 2005). The nematodes were harvested after 48 hours and concentrated into 20ml in vial bottles. Nematode population from each sample was determined using a 1ml aliquot of a wellmixed
suspension
pipetted
into
a
Hawksley’s
nematode counter and enumerated under a Leica MS 15 dissecting microscope. Counting was repeated in three aliquots and the mean recorded. Nematodes extracted from the roots were expressed per gram dry root weight. Nematodes were identified to genus level using the morphological features. A photographic record of the nematode genera was obtained using a digital camera (Leica DFC 280) mounted on a
‡ Gall
index according to Bridge and Page (1980) galling
scale of 0-10 where 1= No galls; 2=1-5%; 3=6-10%; 4=1120%; 5=21-30%; 6=31-40%; 7=41-50%; 8=51-75% and 9=76% of root system and 10=All roots severely knotted and no root system and plant usually dead. Fig. 1. Mean Gall indices‡ on bean roots from farms in eight localities of Kirinyaga and Embu Counties. The significantly higher RKN gall indices Manyatta could be due to the mixed crop farming (beans, tomatoes, squash, egg plants) that is a common practice in the area with most of the crops grown
compound microscope.
being good hosts to root knot nematodes (Silva dos Nematode extraction from the soil Nematodes were extracted from a
Santos et al., 2012; Waceke & Chege In Press; sub-
Weselmael & Maurice 2012). Further, the high RKN
samples using the Modified Extraction Tray method
disease severity in Manyatta and Nembure could be
Waceke
200cm3-soil
Page 64
Int. J. Agron. Agri. R. attributed to the susceptibility of the bean varieties
to the build -up of nematode levels over the seasons
grown in the areas. GLP 2 (Rose coco), GLP24 and
beyond damage thresholds (Omwega et al., 1989). In
GLP1004 bean varieties that are commonly grown in
farms where fertilizers (organic or inorganic) were
the area are more susceptible to RKN than GLP 585
used, lower gall indices were recorded. It has been
(Wairimu) and GLP 92 (Mwitemania) (Omwega et al.,
reported that application of organic amendments and
1989; Silva dos Santos et al., 2012; Weselmael &
fertilizers increases growth and vigor of nematode
Maurice 2012) grown in other localities. The relatively
infected plant thus allowing the host to tolerate
low galling indices some localities could be due to the
nematode attack (Rheenen et al., 1981) while organic
relatively poor bean host of RKN namely GLP 585
matter in the soil allows nematode antagonists to
(Wairimu) and GLP 92 (Mwitemania) that are grown
compete successfully and attack nematodes (Waceke
in the area besides the high use of pesticides and
and Waudo 2002).
organic and inorganic fertilizers. Farming in these localities is semi â&#x20AC;&#x201C; commercial unlike in other areas
Diversity and Density of PPN associated with beans
where farming is purely subsistence.
roots The
most
common
plant
parasitic
nematodes
The high nematode damage and population densities
encountered in bean roots were Meloidogyne spp.
could be due to poor agricultural practices (low or no
Pratylenchus spp. and Scutellonema spp. with a
fertilizer or agricultural inputs and continuous bean
frequency
cropping (twice a year)) in the areas. This contributes
respectively (Table 1).
of
94.38%,
78.25%
and
59.13%,
Table 1. Percent Frequency of occurrence of plant parasitic nematodes in bean roots obtained from 8 localities in Kirinyaga and Embu Counties. Nematode genus Meloidogyne Pratylenchus Scutellonema Hemicycliophora
Kibirigwi 100 80 26
Makutano 100 86 63 -
Kagio 100 88 24 21
Mwea 78 37 62 -
Kutus 98 93 90 -
Nembure 85 84 74 -
Manyatta 100 80 80 -
Runyenjes 94 78 80 -
Hemicycliophora spp was present in two localities;
nematodes than lesion nematodes (Waceke et al.,
Kibirigwi and Kagio with a frequency of occurrence of up
2007; Waceke and Chege 2017 In Press).The
to 26%. Meloidogyne, Pratylenchus and Scutellonema
relatively high densities of Pratylenchus in Nembure
spp. have been reported to be the major nematode
could be attributed to the presence of coffee and
genera associated with beans in different parts of the
maize in most of the farms where beans were
country and so the findings of this study corroborates
intercropped with them (Waceke and Arim 2017; Arim
with the findings by Kimenju et al., 1999.
et al., 2006; Katungi et al., 2010). Coffee and maize are good hosts of Pratylenchus spp and coffee being a
Roots
of
bean
supported
higher
densities
of
perennial crop, it support the continuous growth and
Meloidogyne spp than Pratylenchus spp.in all the
reproduction of the lesion nematodes. Further, lesion
localities except Nembure where the density of lesion
nematodes are polyphagus except P. goodeyi which
nematodes was more than double that of the root
infects
knot nematodes (Table 2). The differences in the
ectoparasites; Scutellonema and Hemicycliophora on
densities of the two nematodes in bean roots could be
bean production needs to be further investigated.
only
bananas.
The
impact
of
the
two
attributed to the difference in their mode of feeding (lesion nematodes are migratory endoparasites while
Overall farms in Kutus, Runyenjes and Manyatta had
root knot nematodes are sedentary endoparasites and
some of the highest nematode densities in bean roots
to the susceptible bean genotype. The bean genotypes
while Mwea, Kibirigwi and Kagio had some of the
grown in the area are more susceptible to root knot
lowest densities (Table 2).
Waceke
Page 65
Int. J. Agron. Agri. R. Most of the farmers in the irrigation schemes
Disease severity and nematode composition and
concentrated in Mwea and Kibirigwi localities are semi
distribution were notably low in the irrigated areas (L1,
commercial farmers and use pesticides, organic and
L3 and L4) compared to rain-fed areas (L2, L5, L6, L7
inorganic fertilizers and practice good crop husbandry in
and L8). This supports the observation that disease
their production systems that could have reduced the
severity is more pronounced under conditions of water
nematode population (Wortmann & Allen 1994).
stress (Rheenen et al, 1981; Wortmann & Allen 1994).
Table 2. Mean Nematodes densities per g dry root weight of bean root in 8 localities in Kirinyaga and Embu Counties. Nematode genus Meloidogyne Pratylenchus Scutellonema Hemicycliophora Total
Kibirigwi 33.6 8.4 5.2 47.2
Makutano 76 16.6 13.8 106.4
Kagio 47 16.2 2.4 4.2 69.8
Diversity and density of PPN in soil Eleven
PPN
genera
Pratylenchus
spp.
Helicotylenchus Tylenchorynchus
namely and
spp.,
Kutus 113.4 29.8 20.6 163.8
Nembure 36.2 84 7.4 127.6
Manyatta 97.4 17.4 20.2 135
Runyenjes 104.8 34.8 12.8 152.4
spp, some of the most frequently encountered had an
Meloidogyne Scutellonema
Paratylenchus
spp.,
Mwea 18.4 12.6 6.8 37.8
Tylenchus
spp.
overall percent occurrence of 100%, 97%, 73% and 63%,
spp.,
respectively (Table 3). All the 11 genera were present in
spp.,
three of the localities; Kibirigwi, Kutus and Nembure.
spp.,
Hemicycliophora spp., Hoplolaimus spp., Trichodorus
This could be attributed to the diversity of the crops
spp. and Xiphinema were encountered in bean
grown in these localities (Katungi et al., 2010). Kagio
rhizosphere soils (Table 3) underscoring the importance
had the lowest diversity of nematodes with seven out
of PPN in crop production systems. Pratylenchus spp,
of the 11 genera being isolated from the farms in this
Meloidogyne spp, Scutellonema spp and Paratylenchus
locality (Table 3).
Table 3. Percent frequency of occurrence of PPN in soil obtained from 8 localities in Kirinyaga and Embu Counties. Nematode genus Meloidogyne Pratylenchus Scutellonema Helicotylenchus Paratylenchus Tylenchohynchus Tylenchus Hemicycliophora Hoplolaimus Trichodorus Xiphinema
Kibirigwi 100 100 70 80 50 70 81 31 33 72 30
Makutano 100 100 63 38 78 25 18 16 24 17
Kagio 100 100 51 23 50 22 50
Mwea 78 100 78 22 57 38 12 36 20
Kutus 100 100 81 82 46 82 48 63 46 100 65
Nembure 100 100 78 62 60 40 79 15 23 62 38
Manyatta 100 100 80 40 80 62 60 60 63 19
Runyenjes 100 100 60 21 81 42 96 40 43
Six of the 11 genera; Meloidogyne, Pratylenchus,
The three localities in Embu (Nembure, Manyatta &
Scutellonema, Helicotylenchus, Paratylenchus and
Runyenjes) had some of the highest nematode
Xiphinema
farms
densities in the soils and nematode diversity (Table 3)
underscoring the importance of PPN in agriculture. The
while Kagio and Mwea had some of the lowest
rich biodiversity could be due to mixed cropping systems
densities (Table 4).
were
encountered in all
the
in most of the localities (Kavuluko et al., 2010). Table 4. Mean population densities of dominant plant parasitic nematodes recovered from 200cm3 of soil samples. Nematode genus Meloidogyne Pratylenchus Scutellonema Paratylenchus Helicotylenchus Total
Waceke
Kibirigwi 266 272 38 34 80 690
Makutano 227 224 75 74 43 643
Kagio 184 201 28 29 11 453
Mwea 158 175 60 37 8 438
Kutus 264 222 77 27 72 662
Nembure 838 491 155 101 72 1657
Manyatta 602 359 174 97 18 1250
Runyenjes 487 285 69 92 14 947
Page 66
Int. J. Agron. Agri. R. The high nematode densities in these areas could be
The study revealed high densities of lesion nematodes
attributed to the mixed cropping practiced in the
(Pratylenchus
area while the low nematode densities in Kagio and
(Meloidogyne spp) in bean roots and soil. Upper
Mwea could be attributed to the application of
Midland 3 (UM3) AEZs and UM4 had higher nematode
pesticides and other inputs. Crop production in this
population densities and diversity than UM2. Disease
area is done on a semi- commercial basis and so
severity and nematode composition and distribution
application of pesticides and other inputs is
were notably lower in the irrigated areas compared to
relatively a more common practice than in other
areas where bean production relies on rain
spp.)
and
root
knot
nematodes
study areas. Some of the farms in these areas were formerly rice paddies and therefore the flooding
Recommendation
previously done could have contributed to the low
Continuous production of susceptible bean varieties
nematode densities. It is notable that these areas
should be minimized to reduce PPN population build
had also the lowest nematode diversity (Table 3).
up and minimize the detrimental effects on the beans. Further selection of the varieties to be grown in the
High counts of lesion nematodes (Pratylenchus spp.)
area should be done carefully. Appropriate measures
recovered from both the soil and root samples further
should be incorporated in the bean production
confirm their association with bean plants. (Wortmann
systems to reduce the high densities of lesion
& Allen 1994)). Scutellonema spp., found in most of the
nematodes (Pratylenchus
localities is a polyphagous genus associated with a wide
nematodes (Meloidogyne spp).
range of plant species including maize and beans (Rheenen et al., 1981). Dominance of Meloidogyne species in all the localities may be attributed to the presence of beans, a suitable host and other alternative hosts (including weeds) and continuous cropping. The wide diversity of nematodes identified from the sampled farms could be due to mixed cropping systems (Rheenen et al., 1981).
and
structure
knot
Acknowledgement I acknowledge the Rockefeller Foundation for funding this project, the farmers for allowing the collection of samples from their farms and Kenyatta University for providing office and laboratory spaces. References Bridge, Page. 1980. Estimation of Root-Knot
Considering the AEZs in relation to the species composition
spp.) and root
of
the
nematode
communities, UM3 and UM4 had higher nematode population densities. This could be due to differences in soil properties and mixed cropping systems common in these AEZs as previously reported by (Wortmann & Allen 1994). Disease severity and nematode composition and distribution were notably low in the irrigated areas Kibirigwi, Kagio and Mwea
Nematode Infestation Levels on Roots Using a Rating Chart. Tropical Pest Management 26(3), 296-298 Hooper DJ, Hallmann J, Subbotin SA. 2005. Methods for extraction, processing and detection of plant and soil nematodes. In: Plant Parasitic Nematodes in Subtropical and Tropical Agriculture 2nd edition. Luc. M., Sikora, R. A. and Bridge, J. (Eds), pg 53-80. CAB international, Oxfordshire U.K.
compared to rain-fed areas such as Makutano,
Jaetzold R, Schmidt H. 1983. Farm Management
Nembure and Manyatta. This supports the observation
Handbook of Kenya. Vol. III Ministry of Agriculture
that disease severity is more pronounced under
Nairobi Kenya.
conditions of water stress (Rheenen et al., 1981). Karanja NK, Kimenju JW, Macharia I, Muiru Conclusion
DM. 2003. Plant parasitic nematode associated with
Manyatta (L7) and Nembure (L6), had the highest
common bean (Phaseolus vulgaris L.) and integrated
and second highest gall indices, respectively while
management
Kibirigwi (L1), Makutano (L2) and Mwea (L4).
Journal 11, 503-510.
Waceke
approaches.
African
Crop
Science
Page 67
Int. J. Agron. Agri. R. Katungi E, Farrow A, Mutuoki T, Gebeyehu S,
Talwana H, Davis KG, Waceke JW, Sibanda Z,
Karanja D, Alemayehu F, Sperling F, Beebe S,
Manzanilla-Lopez R, Kimenju JW, Nessie DL,
Rubyogo RC, Buruchara R. 2010. Improving
Masawe C. 2016. Agricultural nematology in East and
common bean productivity: an analysis of socio-economic
Southern Africa: Problems, Management Strategies
factors in Ethiopia and Eastern Kenya. Baseline Report
and Stakeholder linkages. Pest Management Science
Tropical legumes II. Centro Internacional de Agricultura
72, 226-245.
Tropical - CIAT. Cali Colombia. Kavuluko JM, Gichuki C, Waceke JW, Runo SM. 2010. Characterization of root-knot nematodes (Meloidogyne spp.) from selected legumes in Mbeere District Kenya using isoenzyme phenotypes. In â&#x20AC;&#x153;Transforming Agriculture for improved livelihoods through Agricultural Product Value Chains: The Proceedings of the 12th KARI Biennial Scientific Conferenceâ&#x20AC;?8- 12th Nov 2010 Nairobi Kenya Pg. 92- 97.
Waceke JW, Arim JO, Waudo SW, Kimenju JW. 2007. Impact of some soil fertility management practices on lesion nematodes of maize in Kenya. First Biennual Meeting of the Regional Universities Forum for Capacity Building In Agriculture, 23-27 April 2007, Mangochi, Malawi pp 179-186. Waceke JW, Arim OJ. 2017. Management of lesion nematodes on maize using green and cattle manures in
Kimenju JW, Karanja NK, Macharia I. 1999.
the Central Highlands of Kenya. International Journal of
Plant parasitic nematodes associated with common
Agriculture, Environment and Bioresearch 2(6), 52-66.
beans in Kenya and the effect of Meloidogyne infection on bean nodulation. African Crop Science Journal 7, 503-510.
Waceke JW, Chege FN. 2017. Response of common beans to a mixed population of Meloidogyne javanica and Meloidogyne arenaria (Root Knot
Mwaniki A. 2015. Assessment of Bean Production Constraints and Seed Quality and Health of Improved Common Bean Seed. African Crop Science Journal 13, 116-121.
Nematodes) In Central Highlands of Kenya. In Press. Waceke JW, Waudo SW. 2001. Effect of time on efficacy
of
Meloidogyne
Omwega CO, Thomason IJ, Roberts P, Waines
organic
soil
incognita
on
amendments okra.
against
East
Africa
Agriculture and Forestry Journal 67(1), 19-29.
CG. 1989. Identification of new sources of resistance to the root knot nematodes in Phaseolus. Crop
Wesemael WM, Maurice M. 2012. Screening of common bean (Phaseoulus vulgaris L.) for resistance
science 29, 1463-1468.
against temperate root-knot nematodes (Meloidogyne Rheenen HA, VanHassebach OE, Mungai SGS.
spp). Pest Management Science 68, 702-708.
1981. The effects of growing beans together with maize on incidence of bean diseases and pest.
Wortmann CS, Allen DJ. 1994. Africa bean
Netherlands Journal of Plant pathology 87,193-199.
production
Silva dos Santos LN, Alves FR, Belan LL, Cabral PDS, Matta FP, Junior WCJ, Moraes WB. 2012. Damage quantification and reaction of bean
genotypes
(Phaseolus
vulgaris
L.)
environments:
their
definition,
characteristics and constraints. Network on Bean Research in Africa, Occasional Paper Series No.11, CIAT, Dar-es-saalam.
to
Meloidogyne incognita race 3 and Meloidogyne. javanica. Summa Phytopathol Botucatu 38, 24-29.
Waceke
Page 68